The S. cerevisiae SUMO stress response is a conjugation-deconjugation cycle that targets the transcription machinery

Journal of Proteomics

Volumn 118, Issue , 2015, Pages 39-48

  Lewicki, Megan C ^a   Srikumar, Tharan ^a   Johnson, Erica ^b   Raught, Brian ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Affinity purification coupled with mass spectrometry (AP MS); Environmental stress; SUMO

Indexed keywords

CYC8 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; PROTEINASE; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SUMO 1 PROTEIN; TUP1 PROTEIN, S CEREVISIAE; ULP2 PROTEIN, S CEREVISIAE;

GENETICS; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ENDOPEPTIDASES; HUMANS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; SUMO-1 PROTEIN;

EID: 84940001123     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.11.012     Document Type: Article

References (50)

1. Johnson E.S. Protein modification by SUMO. Annu Rev Biochem 2004, 73:355-382.
2. Kerscher O., Felberbaum R., Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 2006, 22:159-180.
3. Makhnevych T., Sydorskyy Y., Xin X., Srikumar T., Vizeacoumar F.J., Jeram S.M., et al. Global map of SUMO function revealed by protein-protein interaction and genetic networks. Mol Cell 2009, 33:124-135.
4. Srikumar T., Lewicki M.C., Costanzo M., Tkach J.M., van Bakel H., Tsui K., et al. Global analysis of SUMO chain function reveals multiple roles in chromatin regulation. J Cell Biol 2013, 201:145-163.
5. Yeh E.T. SUMOylation and De-SUMOylation: wrestling with life's processes. J Biol Chem 2009, 284:8223-8227.
6. Flotho A., Melchior F. Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem 2013, 82:357-385.
7. Tempe D., Piechaczyk M., Bossis G. SUMO under stress. Biochem Soc Trans 2008, 36:874-878.
8. Zhou W., Ryan J.J., Zhou H. Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 2004, 279:32262-32268.
9. Sydorskyy Y., Srikumar T., Jeram S.M., Wheaton S., Vizeacoumar F.J., Makhnevych T., et al. A novel mechanism for SUMO system control: regulated Ulp1 nucleolar sequestration. Mol Cell Biol 2010, 30:4452-4462.
10. Castro P.H., Tavares R.M., Bejarano E.R., Azevedo H. SUMO, a heavyweight player in plant abiotic stress responses. Cell Mol Life Sci 2012, 69:3269-3283.
11. Catala R., Ouyang J., Abreu I.A., Hu Y., Seo H., Zhang X., et al. The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 2007, 19:2952-2966.
12. Elrouby N., Coupland G. Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proc Natl Acad Sci U S A 2010, 107:17415-17420.
13. Kurepa J., Walker J.M., Smalle J., Gosink M.M., Davis S.J., Durham T.L., et al. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 2003, 278:6862-6872.
14. Manza L.L., Codreanu S.G., Stamer S.L., Smith D.L., Wells K.S., Roberts R.L., et al. Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chem Res Toxicol 2004, 17:1706-1715.
15. Saitoh H., Hinchey J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 2000, 275:6252-6258.
16. Golebiowski F., Matic I., Tatham M.H., Cole C., Yin Y., Nakamura A., et al. System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2009, 2:ra24.
17. Wang L., Ma Q., Yang W., Mackensen G.B., Paschen W. Moderate hypothermia induces marked increase in levels and nuclear accumulation of SUMO2/3-conjugated proteins in neurons. J Neurochem 2012, 123:349-359.
18. Wang Z., Wang R., Sheng H., Sheng S.P., Paschen W., Yang W. Transient ischemia induces massive nuclear accumulation of SUMO2/3-conjugated proteins in spinal cord neurons. Spinal Cord 2013, 51:139-143.
19. Yang W., Sheng H., Warner D.S., Paschen W. Transient global cerebral ischemia induces a massive increase in protein sumoylation. J Cereb Blood Flow Metab 2008, 28:269-279.
20. Krumova P., Weishaupt J.H. Sumoylation in neurodegenerative diseases. Cell Mol Life Sci 2013, 70:2123-2138.
21. Dorval V., Fraser P.E. SUMO on the road to neurodegeneration. Biochim Biophys Acta 2007, 1773:694-706.
22. Baczyk D., Drewlo S., Kingdom J.C. Emerging role of SUMOylation in placental pathology. Placenta 2013, 34:606-612.
23. Delorme E. Transformation of Saccharomyces cerevisiae by electroporation. Appl Environ Microbiol 1989, 55:2242-2246.
24. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Seraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 1999, 17:1030-1032.
25. Craig R., Beavis R.C. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 2004, 20:1466-1467.
26. Eng J.K., Jahan T.A., Hoopmann M.R. Comet: an open-source MS/MS sequence database search tool. Proteomics 2013, 13:22-24.
27. Shteynberg D., Deutsch E.W., Lam H., Eng J.K., Sun Z., Tasman N., et al. iProphet: multi-level integrative analysis of shotgun proteomic data improves peptide and protein identification rates and error estimates. Mol Cell Proteomics 2011, 10:M111. [007690].
28. Choi H., Larsen B., Lin Z.Y., Breitkreutz A., Mellacheruvu D., Fermin D., et al. SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat Methods 2011, 8:70-73.
29. Mnaimneh S., Davierwala A.P., Haynes J., Moffat J., Peng W.T., Zhang W., et al. Exploration of essential gene functions via titratable promoter alleles. Cell 2004, 118:31-44.
30. Reindle A., Belichenko I., Bylebyl G.R., Chen X.L., Gandhi N., Johnson E.S. Multiple domains in Siz SUMO ligases contribute to substrate selectivity. J Cell Sci 2006, 119:4749-4757.
31. Perry J.J., Tainer J.A., Boddy M.N. A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci 2008, 33:201-208.
32. Prudden J., Pebernard S., Raffa G., Slavin D.A., Perry J.J., Tainer J.A., et al. SUMO-targeted ubiquitin ligases in genome stability. EMBO J 2007, 26:4089-4101.
33. Uzunova K., Gottsche K., Miteva M., Weisshaar S.R., Glanemann C., Schnellhardt M., et al. Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 2007, 282:34167-34175.
34. Collins G.A., Gomez T.A., Deshaies R.J., Tansey W.P. Combined chemical and genetic approach to inhibit proteolysis by the proteasome. Yeast 2010, 27:965-974.
35. Berry D.B., Gasch A.P. Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol Biol Cell 2008, 19:4580-4587.
36. Guan Q., Haroon S., Bravo D.G., Will J.L., Gasch A.P. Cellular memory of acquired stress resistance in Saccharomyces cerevisiae. Genetics 2012, 192:495-505.
37. Li S.J., Hochstrasser M. A new protease required for cell-cycle progression in yeast. Nature 1999, 398:246-251.
38. Bylebyl G.R., Belichenko I., Johnson E.S. The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J Biol Chem 2003, 278:44113-44120.
39. Denison C., Rudner A.D., Gerber S.A., Bakalarski C.E., Moazed D., Gygi S.P. A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol Cell Proteomics 2005, 4:246-254.
40. Hannich J.T., Lewis A., Kroetz M.B., Li S.J., Heide H., Emili A., et al. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 2005, 280:4102-4110.
41. Panse V.G., Hardeland U., Werner T., Kuster B., Hurt E. A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 2004, 279:41346-41351.
42. Wohlschlegel J.A., Johnson E.S., Reed S.I., Yates J.R. Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 2004, 279:45662-45668.
43. Malave T.M., Dent S.Y. Transcriptional repression by Tup1-Ssn6. Biochem Cell Biol 2006, 84:437-443.
44. Srikumar T., Lewicki M.C., Raught B. A global S. cerevisiae small ubiquitin-related modifier (SUMO) system interactome. Mol Syst Biol 2013, 9:668.
45. Grigull J., Mnaimneh S., Pootoolal J., Robinson M.D., Hughes T.R. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol Cell Biol 2004, 24:5534-5547.
46. Tipper D.J. Inhibition of yeast ribonucleic acid polymerases by thiolutin. J Bacteriol 1973, 116:245-256.
47. Lyst M.J., Stancheva I. A role for SUMO modification in transcriptional repression and activation. Biochem Soc Trans 2007, 35:1389-1392.
48. Neyret-Kahn H., Benhamed M., Ye T., Le Gras S., Cossec J.C., Lapaquette P., et al. Sumoylation at chromatin governs coordinated repression of a transcriptional program essential for cell growth and proliferation. Genome Res 2013, 23:1563-1579.
49. Rosonina E., Duncan S.M., Manley J.L. SUMO functions in constitutive transcription and during activation of inducible genes in yeast. Genes Dev 2010, 24:1242-1252.
50. Gasch A.P., Spellman P.T., Kao C.M., Carmel-Harel O., Eisen M.B., Storz G., et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11:4241-4257.